Genome mining of nonenzymatic ortho-quinone methide-based pseudonatural products from ascidian-derived fungus Diaporthe sp.SYSU-MS4722

Bioorg Chem. 2025 Jan:154:108081. doi: 10.1016/j.bioorg.2024.108081. Epub 2024 Dec 23.

Abstract

Ortho-quinone methides (o-QMs), generated by oxidative dehydration of clavatol, are highly reactive intermediates in biosynthesis that give rise to a variety of clavatol-containing pseudonatural products (PNPs) in fungi through intra- and intermolecular nonenzymatic cyclization/addition reaction, and some compounds have significant biological activities. Here we report our genome mining efforts on a cryptic clavatol biosynthetic gene cluster (BGC) from an ascidian-derived fungus Diaporthe sp. SYSU-MS4722. The core genes NR-PKS (DiaG), Esterase (DiaF) derived from the fungus Diaporthe sp. SYSU-MS4722 clavatol BGC and the known α-ketoglutarate-dependent nonheme iron enzymes (ClaD) were heterologously expressed in the Aspergillus oryzae NSAR1 (A. oryzae NSAR1). Thirteen new monomeric, dimeric, and trimeric clavatol-based PNPs (7-19), together with three known compounds (20-22) were isolated from the above transformant. Their structures including absolute configurations were elucidated by spectroscopic analysis (UV, IR, HR-ESI-MS, 1D and 2D NMR data), complemented with the X-ray crystallography, the comparison of the experimental and calculated ECD spectra, and gauge-independent atomic orbital (GIAO) NMR calculations. Based on the structural characteristics, their plausible biosynthetic pathways were proposed. Notably, Compounds 8, 9, 14 and 16 exhibited potent anti-fibrotic activity with EC50 values of 28.9, 10.0, 3.5 and 30.1 μM, respectively.

Keywords: Anti-fibrotic activity; Aspergillus oryzae NSAR1; Genome mining; Heterologous expression; clavatol-based PNPs.

MeSH terms

  • Animals
  • Ascomycota / chemistry
  • Ascomycota / genetics
  • Ascomycota / metabolism
  • Aspergillus oryzae / genetics
  • Biological Products / chemistry
  • Biological Products / metabolism
  • Biological Products / pharmacology
  • Dose-Response Relationship, Drug
  • Humans
  • Indolequinones* / chemistry
  • Molecular Structure
  • Structure-Activity Relationship
  • Urochordata / microbiology

Substances

  • quinone methide
  • Indolequinones
  • Biological Products